Contribution of inflammation and impaired angiogenesis to the pathobiology of chronic thromboembolic pulmonary hypertension

European Respiratory Journal

Volumn 46, Issue 2, 2015, Pages 431-443

  Quarck, Rozenn ^a   Wynants, Marijke ^a   Verbeken, Erik ^a   Meyns, Bart ^b   Delcroix, Marion ^b  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b UNIVERSITY HOSPITALS LEUVEN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

C REACTIVE PROTEIN; COLLAGEN; ELASTIN; FIBRIN; GELATINASE B; INTERLEUKIN 10; LIPID; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MONOCYTE CHEMOTACTIC PROTEIN 1; BIOLOGICAL MARKER; CCL2 PROTEIN, HUMAN; CCL3 PROTEIN, HUMAN; IL10 PROTEIN, HUMAN; MMP9 PROTEIN, HUMAN;

ADULT; ADVERSE OUTCOME; ANGIOGENESIS; ARTICLE; ATHEROSCLEROSIS; B LYMPHOCYTE; BIOACCUMULATION; CHRONIC THROMBOEMBOLIC PULMONARY HYPERTENSION; CONTROLLED STUDY; DISEASE SEVERITY; ENDARTERECTOMY; ENDOTHELIUM CELL; FEMALE; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; INFLAMMATION; INFLAMMATORY CELL; INFLAMMATORY INFILTRATE; MACROPHAGE; MAJOR CLINICAL STUDY; MALE; NEOINTIMA; NEUTROPHIL; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PULMONARY ENDARTERECTOMY; PULMONARY HYPERTENSION; SMOOTH MUSCLE FIBER; SURVIVAL RATE; T LYMPHOCYTE; THROMBOSIS; BLOOD; CHRONIC DISEASE; COMPLICATION; DISEASE COURSE; HYPERTENSION, PULMONARY; KAPLAN MEIER METHOD; LUNG EMBOLISM; MIDDLE AGED; PATHOLOGY; PULMONARY ARTERY;

BIOMARKERS; C-REACTIVE PROTEIN; CHEMOKINE CCL2; CHEMOKINE CCL3; CHRONIC DISEASE; DISEASE PROGRESSION; ENDARTERECTOMY; FEMALE; HUMANS; HYPERTENSION, PULMONARY; INFLAMMATION; INTERLEUKIN-10; KAPLAN-MEIER ESTIMATE; MALE; MATRIX METALLOPROTEINASE 9; MIDDLE AGED; NEOVASCULARIZATION, PHYSIOLOGIC; PULMONARY ARTERY; PULMONARY EMBOLISM;

EID: 84938840963     PISSN: 09031936     EISSN: 13993003     Source Type: Journal    
DOI: 10.1183/09031936.00009914     Document Type: Article

References (49)

1. Moser KM, Bloor CM. Pulmonary vascular lesions occurring in patients with chronic major vessel thromboembolic pulmonary hypertension. Chest 1993; 103: 685-692.
2. McNeil K, Dunning J. Chronic thromboembolic pulmonary hypertension (CTEPH). Heart 2007; 93: 1152-1158.
3. Hoeper MM, Mayer E, Simonneau G, et al. Chronic thromboembolic pulmonary hypertension. Circulation 2006; 113: 2011-2020.
4. Thistlethwaite PA, Mo M, Madani MM, et al. Operative classification of thromboembolic disease determines outcome after pulmonary endarterectomy. J Thorac Cardiovasc Surg 2002; 124: 1203-1211.
5. Arbustini E, Morbini P, D'Armini AM, et al. Plaque composition in plexogenic and thromboembolic pulmonary hypertension: the critical role of thrombotic material in pultaceous core formation. Heart 2002; 88: 177-182.
6. Bernard J, Yi ES. Pulmonary thromboendarterectomy: a clinicopathologic study of 200 consecutive pulmonary thromboendarterectomy cases in one institution. Hum Pathol 2007; 38: 871-877.
7. Bonderman D, Jakowitsch J, Adlbrecht C, et al. Medical conditions increasing the risk of chronic thromboembolic pulmonary hypertension. Thromb Haemost 2005; 93: 512-516.
8. Bonderman D, Jakowitsch J, Redwan B, et al. Role for Staphylococci in misguided thrombus resolution of chronic thromboembolic pulmonary hypertension. Arterioscler Thromb Vasc Biol 2008; 28: 678-684.
9. Frey MK, Alias S, Winter MP, et al. Splenectomy is modifying the vascular remodeling of thrombosis. J Am Heart Assoc 2014; 3: e000772.
10. Langer F, Schramm R, Bauer M, et al. Cytokine response to pulmonary thromboendarterectomy. Chest 2004; 126: 135-141.
11. Kimura H, Okada O, Tanabe N, et al. Plasma monocyte chemoattractant protein-1 and pulmonary vascular resistance in chronic thromboembolic pulmonary hypertension. Am J Respir Crit Care Med 2001; 164: 319-324.
12. Soon E, Holmes A, Treacy CM, et al. Inflammatory cytokines are elevated in patients with operable chronic thromboembolic pulmonary hypertension and predict outcome post-endarterectomy. Am J Respir Crit Care Med 2011; 183: A2287.
13. Sungprem K, Khongphatthanayothin A, Kiettisanpipop P, et al. Serum level of soluble intercellular adhesion molecule-1 correlates with pulmonary arterial pressure in children with congenital heart disease. Pediatr Cardiol 2009; 30: 472-476.
14. Fartoukh M, Emilie D, Le Gall C, et al. Chemokine macrophage inflammatory protein-1α mRNA expression in lung biopsy specimens of primary pulmonary hypertension. Chest 1998; 114: 50S-51S.
15. Schumann C, Lepper PM, Frank H, et al. Circulating biomarkers of tissue remodelling in pulmonary hypertension. Biomarkers 2010; 15: 523-532.
16. Tuder RM, Chacon M, Alger L, et al. Expression of angiogenesis-related molecules in plexiform lesions in severe pulmonary hypertension: evidence for a process of disordered angiogenesis. J Pathol 2001; 195: 367-374.
17. Quarck R, Nawrot T, Meyns B, et al. C-reactive protein: a new predictor of adverse outcome in pulmonary arterial hypertension. J Am Coll Cardiol 2009; 53: 1211-1218.
18. Wynants M, Quarck R, Ronisz A, et al. Effects of C-reactive protein on human pulmonary vascular cells in chronic thromboembolic pulmonary hypertension. Eur Respir J 2012; 40: 886-894.
19. Wynants M, Vengethasamy L, Ronisz A, et al. NF-κB pathway is involved in CRP-induced effects on pulmonary arterial endothelial cells in chronic thromboembolic pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol 2013; 305: L934-L942.
20. Lang IM, Pesavento R, Bonderman D, et al. Risk factors and basic mechanisms of chronic thromboembolic pulmonary hypertension: a current understanding. Eur Respir J 2013; 41: 462-468.
21. Waltham M, Burnand KG, Collins M, et al. Vascular endothelial growth factor and basic fibroblast growth factor are found in resolving venous thrombi. J Vasc Surg 2000; 32: 988-996.
22. Waltham M, Burnand KG, Collins M, et al. Vascular endothelial growth factor enhances venous thrombus recanalisation and organisation. Thromb Haemost 2003; 89: 169-176.
23. Alias S, Redwan B, Panzenböck A, et al. Defective angiogenesis delays thrombus resolution: a potential pathogenetic mechanism underlying chronic thromboembolic pulmonary hypertension. Arterioscler Thromb Vasc Biol 2014; 34: 810-819.
24. Thistlethwaite PA, Mo M, Madani MM, et al. Operative classification of thromboembolic disease determines outcome after pulmonary endarterectomy. J Thorac Cardiovasc Surg 2002; 124: 1203-1211.
25. Skoro-Sajer N, Marta G, Gerges C, et al. Surgical specimens, haemodynamics and long-term outcomes after pulmonary endarterectomy. Thorax 2014; 69: 116-122.
26. Blauwet LA, Edwards WD, Tazelaar HD, et al. Surgical pathology of pulmonary thromboendarterectomy: a study of 54 cases from 1990 to 2001. Hum Pathol 2003; 34: 1290-1298.
27. Pepke-Zaba J, Delcroix M, Lang I, et al. Chronic thromboembolic pulmonary hypertension (CTEPH): results from an international prospective registry. Circulation 2011; 124: 1973-1981.
28. Owens GK, Kumar MS, Wamhoff BR. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev 2004; 84: 767-801.
29. Sobue K, Hayashi K, Nishida W. Molecular mechanism of phenotypic modulation of smooth muscle cells. Horm Res 1998; 50: Suppl. 2, 15-24.
30. Firth AL, Yao W, Ogawa A, et al. Multipotent mesenchymal progenitor cells are present in endarterectomized tissues from patients with chronic thromboembolic pulmonary hypertension. Am J Physiol Cell Physiol 2010; 298: C1217-C1225.
31. Yao W, Firth AL, Sacks RS, et al. Identification of putative endothelial progenitor cells (CD34+CD133+Flk-1+) in endarterectomized tissue of patients with chronic thromboembolic pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol 2009; 296: L870-L878.
32. Humbert M, Morrell NW, Archer SL, et al. Cellular and molecular pathobiology of pulmonary arterial hypertension. J Am Coll Cardiol 2004; 43: 13S-24S.
33. Hassoun PM, Mouthon L, Barber JA, et al. Inflammation, growth factors, and pulmonary vascular remodeling. J Am Coll Cardiol 2009; 54: S10-S19.
34. Haoming S, Lemin W, Zhu G, et al. T cell-mediated immune deficiency or compromise in patients with CTEPH. Am J Respir Crit Care Med 2011; 183: 417-418.
35. Frey MK, Alias S, Winter MP, et al. Splenectomy is modifying the vascular remodeling of thrombosis. J Am Heart Assoc 2014; 3: e000772.
36. Kabutomori O, Kanakura Y, Iwatani Y. Movement of toxic granulation neutrophils and C-reactive protein in inflammatory processes. Am J Med 2002; 112: 595-596.
37. Kabutomori O, Iwatani Y, Kanakura Y. Toxic granulation neutrophils and C-reactive protein. Arch Intern Med 2000; 160: 3326-3327.
38. Bisoendial RJ, Birjmohun RS, Akdim F, et al. C-reactive protein elicits white blood cell activation in humans. Am J Med 2009; 122: 582.e1-9.
39. Heuertz RM, Tricomi SM, Ezekiel UR, et al. C-reactive protein inhibits chemotactic peptide-induced p38 mitogen-activated protein kinase activity and human neutrophil movement. J Biol Chem 1999; 274: 17968-17974.
40. Zhong W, Zen Q, Tebo J, et al. Effect of human C-reactive protein on chemokine and chemotactic factor-induced neutrophil chemotaxis and signaling. J Immunol 1998; 161: 2533-2540.
41. Inoue T, Kato T, Uchida T, et al. Local release of C-reactive protein from vulnerable plaque or coronary arterial wall injured by stenting. J Am Coll Cardiol 2005; 46: 239-245.
42. Abe N, Osanai T, Fujiwara T, et al. C-reactive protein-induced upregulation of extracellular matrix metalloproteinase inducer in macrophages: inhibitory effect of fluvastatin. Life Sci 2006; 78: 1021-1028.
43. Johnson C, Sung HJ, Lessner SM, et al. Matrix metalloproteinase-9 is required for adequate angiogenic revascularization of ischemic tissues: potential role in capillary branching. Circ Res 2004; 94: 262-268.
44. Modarai B, Burnand KG, Humphries J, et al. The role of neovascularisation in the resolution of venous thrombus. Thromb Haemost 2005; 93: 801-809.
45. Zabini D, Nagaraj C, Stacher E, et al. Angiostatic factors in the pulmonary endarterectomy material from chronic thromboembolic pulmonary hypertension patients cause endothelial dysfunction. PLoS One 2012; 7: e43793.
46. Pulido T, Adzerikho I, Channick RN, et al. Macitentan and morbidity and mortality in pulmonary arterial hypertension. N Engl J Med 2013; 369: 809-818.
47. Rahnavardi M, Yan TD, Cao C, et al. Pulmonary thromboendarterectomy for chronic thromboembolic pulmonary hypertension: a systematic review. Ann Thorac Cardiovasc Surg 2011; 17: 435-445.
48. Hoey ET, Mirsadraee S, Pepke-Zaba J, et al. Dual-energy CT angiography for assessment of regional pulmonary perfusion in patients with chronic thromboembolic pulmonary hypertension: initial experience. AJR Am J Roentgenol 2011; 196: 524-532.
49. Dorfmüller P, Günther S, Ghigna MR, et al. Microvascular disease in chronic thromboembolic pulmonary hypertension: a role for pulmonary veins and systemic vasculature. Eur Respir J 2014; 44: 1275-1288.